Structure of a serine protease poised to resynthesize a peptide bond

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 27, 2009, Pages 11034-11039

  Zakharova, Elena ^a   Horvath, Martin P ^a   Goldenberg, David P ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

Bovine pancreatic trypsin inhibitor; Enzyme mechanisms; Trypsin

Indexed keywords

APROTININ; SERINE PROTEINASE; TRYPSIN;

ARTICLE; CATALYSIS; CHEMICAL BOND; CHEMICAL REACTION; COW; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME STRUCTURE; ENZYME SYNTHESIS; HYDROGEN BOND; HYDROLYSIS; MOLECULAR INTERACTION; MOTION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; APROTININ; BIOCATALYSIS; CATTLE; HYDROGEN BONDING; HYDROLYSIS; MODELS, MOLECULAR; PEPTIDES; PROTEIN STRUCTURE, SECONDARY; RATS; TRYPSIN;

BOVINAE;

EID: 67650500717     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0902463106     Document Type: Article

References (51)

1. Page MJ, Di Cera E (2008) Serine peptidases: Classification, structure, and function. Cell Mol Life Sci 65:1220-1236.
2. Ross J, Jiang H, Kanost MR,Wang Y (2003) Serine proteases and their homologs in the Drosophila melanogaster genome: An initial analysis of sequence conservation and phylogenetic relationships. Gene 304:117-131.
3. Puente XS, Sá nchez LM, Overall CM, López-Otín C (2003) Human and mouse proteases: A comparative genomic approach. Nat Rev Genet 4:544-558.
4. Hedstrom L (2002) Serine protease mechanism and specificity. Chem Rev 102:4501-4523.
5. Dodson G, Wlodawer A (1998) Catalytic triads and their relatives. Trends Biochem Sci 23:347-352.
6. Frey PA, Whitt SA, Tobin JB (1994) A low-barrier hydrogen bond in the catalytic triad of serine proteases. Science 264:1927-1930.
7. Warshel A, Papazyan A (1996) Energy considerations show that low-barrier hydrogen bonds do not offer a catalytic advantage over ordinary hydrogen bonds. Proc Natl Acad Sci USA 93:13665-13670.
8. Huber R, et al. (1974) Structure of the complex formed by bovine trypsin and bovine pancreatic trypsin inhibitor. II. Crystallographic refinement at 1.9-Å resolution. J Mol Biol 89:73-101.
9. Read RJ, James MNG (1986) in Proteinase Inhibitors, eds Barrett A, Salvesen G (Elsevier, Amsterdam), pp 301-336.
10. Ding X, Rasmussen BF, Petsko GA, Ringe D (1994) Direct structural observation of an acyl-enzyme intermediate in the hydrolysis of an ester substrate by water. Biochemistry 33:9285-9293.
11. Blanchard H, JamesMNG(1994)Acrystallographic reinvestigation into the structure of Streptomyces griseus proteinase A reveals an acyl-enzyme intermediate. J Mol Biol 241:574-587.
12. Katona G, et al. (2002) X-ray structure of a serine protease acyl-enzyme complex at 95-Å resolution. J Biol Chem 227:21962-21970.
13. Radisky ES, Lee JM, Lu CJK, Koshland DE, Jr (2006) Insights into the serine protease mechanism from atomic-resolution structures of trypsin reaction intermediates. Proc Natl Acad Sci USA 103:6835-6840.
14. Brady K, Wei A, Ringe D, Abeles RH (1990) Structure of chymotrypsin-trifluoromethyl ketone inhibitor complexes: Comparison of slowly and rapidly equilibrating inhibitors. Biochemistry 29:7600-7607.
15. Bone R, Sampson NS, Bartlett PA, Agard DA (1991) Crystal structures of α-lytic protease complexes with irreversibly bound phosphonate esters. Biochemistry 30:2263-2272.
16. Katz BA, Finer-Moore J, Mortezaei R, Rich DH, Stroud RM (1995) Episelection: Novel ki ∼ nanomolar inhibitors of sering proteases selected by binding or chemistry on an enzyme surface. Biochemistry 34:8264-8280.
17. Neidhart D, et al. (2001) Correlation of low-barrier hydrogen bonding and oxyanion binding in transition-state analogue complexes of chymotrypsin. Biochemistry 40:2439-2447.
18. James MNG, Sielecki AR, Brayer GD, Delbaere LTJ, Bauer CA (1980) Structures of product and inhibitor complexes of Streptomyces griseus protease A at 1.8-Å resolution: A model for serine protease catalysis. J Mol Biol 144:43-88.
19. DixonMM,Brennan RG, MatthewsBW(1991) Structure of γ-chymotrypsin in the range pH 2.0 to pH 10.5 suggests that γ-chymotrypsin is a covalent acyl-enzyme adduct at low pH. Int J Biol Macromol 13:89-96.
20. Lee TW, James MNG (2008) 1.2-Å-resolution crystal structures reveal the second tetrahedral intermediates of streptogrisin B (SGPB). Biochim Biophys Acta 1784:319-334.
21. Finkenstadt WR, Laskowski M, Jr (1967) Resynthesis by trypsin of the cleaved peptide bond in modified soybean trypsin inhibitor. J Biol Chem 4:771-773.
22. Laskowski M, Jr, Kato I (1980) Protein inhibitors of proteinases. Annu Rev Biochem 49:593-626.
23. Bode W, Huber R (1992) Natural proteinase inhibitors and their interactions with proteinases. Eur J Biochem 204:433-451.
24. Otlewski J, Jelen F, Zakrzewska M, Oleksy A (2005) The many faces of protease-protein inhibitor interaction. EMBO J 24:1303-1310.
25. Rawlings ND, Tolle DP, Barrett AJ (2004) Evolutionary families of peptidase inhibitors. Biochem J 378:705-716.
26. Longstaff C, Campbell AF, Fersht AR (1990) Recombinant chymotrypsin inhibitor 2: Expression, kinetic analysis of inhibition with α-chymotrypsin and wild-type and mutant subtilisin bpn' and protein engineering to investigate inhibitory specificity and mechanism. Biochemistry 29:7339-7347.
27. Lu WY, et al. (2000) Deciphering the role of the electrostatic interactions involving Gly70 in elgin c by total chemical protein synthesis. Biochemistry 39:3575-3584.
28. Peräkylä M, Kollman PA (2000) Why does trypsin cleave BPTI so slowly? J AmChem Soc 122:3436-3444.
29. Radisky ES, Koshland DE, Jr (2002)Aclogged gutter mechanism for protease inhibitors. Proc Natl Acad Sci USA 99:10316-10321.
30. Ascenzi P, et al. (2003) The bovine basic pancreatic trypsin inhibitor (Kunitz inhibitor): A milestone protein. Curr Protein Pept Sci 4:231-251.
31. Jering H, Tschesche H (1976) Preparation and characterization of the active derivative of bovine trypsin-kallikrein inhibitor (kunitz) with the reactive site lysine-15-alanine -16 hydrolyzed. Eur J Biochem 61:443-452.
32. Tschesche H, Kupfer S (1976) Hydrolysis-resynthesis equilibrium of the lysine 15-alanine 16 peptide bond in bovine trypsin inhibitor (kunitz). Hoppe Seylers Z Physiol Chem 357:769-776.
33. Estell DA, Wilson KA, Laskowski M, Jr (1980) Thermodynamics and kinetics of the hydrolysis of the reactive-site peptide bond in pancreatic trypsin inhibitor (Kunitz) by Dermasterias imbricata trypsin 1. Biochemistry 19:131-137.
34. Perona JJ, Tsu CA, Craik CS, Fletterick RJ (1993) Crystal structures of rat anionic trypsin complexed with the protein inhibitors APPI and BPTI. J Mol Biol 230:919-930.
35. Pasternak A, Ringe D, Hedstrom L (1999) Comparison of anionic and cationic trypsinogens: The anionic activation domain is more flexible in solution and differs in its mode of BPTI binding in the crystal structure. Protein Sci 8:253-258.
36. Otting G, Liepinsh E, Wü thrich K (1993) Disulfide bond isomerization in BPTI and BPTI(G36S): An NMR study of correlated mobility in proteins. Biochemistry 32:3571-3582.
37. Millet O, Loria JP, Kroenke CD, Pons M, Palmer AG, III (2000) The static magnetic field dependence of chemical exchange linebroadening defines the NMR chemical shift time scale. J Am Chem Soc 122:2867-2877.
38. Czapinska H, Otlewski J, Krzywda S, Sheldrick GM, Jaskó lski M (2000) High-resolution structure of bovine pancreatic trypsin inhibitor with altered binding loop sequence. J Mol Biol 295:1237-1249.
39. Addlagatta A, Krzywda S, Czapinska H, Otlewski J, Jaskó lski M (2001) Ultrahighresolution structure of a BPTI mutant. Acta Crystallogr D 57:649-663.
40. Singer PT, Smalas A, Carty RP, Mangel WF, Sweet RM (1993) The hydrolytic water molecule in trypsin, revealed by time-resolved Laue crystallography. Science 259:669-673.
41. Perona JJ, Craik CS, Fletterick RJ (1993) Locating the catalytic water molecule in serine proteases. Science 261:620-621.
42. Wilmouth RC, et al. (1997) Structure of a specific acyl-enzyme complex formed between β-casomorphin-7 and porcine pancreatic elastase. Nat Struct Biol 4:456-462.
43. Wang JH (1970) Directional character of proton transfer in enzyme catalysis. Proc Natl Acad Sci USA 66:874-881.
44. 1-H⋯OACHbond: Proposal for reaction-driven ring flip mechanism in serine protease catalysis. Proc Natl Acad Sci USA 97:10371-10376.
45. Zakharova E, Horvath MP, Goldenberg DP (2008) Functional and structural roles of the Cys14-Cys38 disulfide of bovine pancreatic trypsin inhibitor. JMol Biol 382:998-1013.
46. Seeram SS, Hiraga K, Oda K (1997) Resynthesis of reactive site peptide bond and temporary inhibition of Streptomyces metalloproteinase inhibitor. J Biochem 122:788-794.
47. Albery WJ, Knowles JR (1976) Evolution of enzyme function and the development of catalytic efficiency. Biochemistry 15:5631-5640.
48. Hedstrom L, Szilagyi L, Rutter WJ (1992) Converting trypsin to chymotrypsin: The role of surface loops. Science 255:1249-1253.
49. Pasternak A, Liu X, Lin T, Hedstrom L (1998) Activating a zymogen without proteolytic processing: Mutation of Lys15 and Asn194 activates trypsinogen. Biochemistry 37:16201-16210.
50. Brünger AT, et al. (1998) Crystallography and NMR System: A new software suite for macromolecular structure determination. Acta Crystallogr D 54:905-921.
51. Jones TA, Zou JY, Cowan SW (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47:110-119.